Neurol Sci (2012) 33:689694 DOI 10.

1007/s10072-011-0826-7

BRIEF COMMUNICATION

Observational study of sleep-related disorders in Italian patients with Parkinsons disease: usefulness of the Italian version of Parkinsons disease sleep scale
M. T. Pellecchia A. Antonini U. Bonuccelli G. Fabbrini L. Ferini Strambi F. Stocchi A. Battaglia P. Barone

Received: 20 April 2011 / Accepted: 10 October 2011 / Published online: 3 November 2011 Springer-Verlag 2011

Abstract Sleep disturbances are common in patients with Parkinsons disease (PD). We aimed to evaluate prevalence and severity of nighttime sleep disturbances in Italian PD patients and to validate the Italian version of the Parkinsons disease sleep scale. A total of 221 PD patients and 57 healthy controls participated in a cross-sectional study with retest. PDSS, Epworth Sleepiness Scale (ESS), Hamilton Depression Rating Scale, Unied Parkinsons Disease Rating Scale (UPDRS), and Hoehn and Yahr staging were applied. PDSS total and individual items scores from patients were signicantly lower than those in controls. Internal consistency of PDSS scale was satisfactory and intraclass correlation coefcient for testretest reliability was 0.96 for total PDSS score. A signicant negative correlation was found between total PDSS and ESS scores, and between total PDSS and HDRS scores. PDSS scores were also related to UPDRS sections II, III and IV, and H&Y stage. PDSS and ESS scores were not related to
Electronic supplementary material The online version of this article (doi:10.1007/s10072-011-0826-7) contains supplementary material, which is available to authorized users.
M. T. Pellecchia P. Barone (&) Department of Neurological Sciences, University of Naples, Federico II, Naples, Italy e-mail: barone@unina.it A. Antonini Department for Parkinsons Disease, IRCCS San Camillo, Venice, Italy U. Bonuccelli Department of Neuroscience, University of Pisa, Pisa, Italy G. Fabbrini Department of Neurology and Psychiatry and Neuromed Institute, Sapienza University of Rome, Rome, Italy

levodopa equivalent dose. Daytime sleepiness, depressive symptoms and disease severity correlate with sleep disturbances in Italian PD patients. The PDSS is a valid and reliable tool to evaluate sleep disturbances in Italian patients. Keywords Parkinsons disease Sleep disturbances PDSS ESS

Introduction Sleep disturbances are common in Parkinsons disease (PD), with a prevalence ranging from 60 to 90% of patients, with both impairment of nighttime sleep and excessive daytime sleepiness [1]. Many factors have been implicated including the use of dopaminergic therapy [2], coexisting depression [3], and more importantly the underlying disease itself [46]. Sleep disorders in PD appear to arise from a combination of neurochemical and neurodegenerative changes in central sleep regulatory centres [79].
L. Ferini Strambi Sleep Disorder Center, Division of Neurosciences, ` Vita-Salute San Raffaele, Milan, Italy Universita F. Stocchi Department of Neurology, Institute of Research and Medical Care, IRCCS San Raffaele Roma, Rome, Italy A. Battaglia Pzer Italia, Medical Department, Rome, Italy P. Barone Center for Diagnosis and Treatment of Neurodegenerative Disorders, University of Salerno, Salerno, Italy

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Antiparkinsonian medications may affect sleep since they act on motor and non-motor symptoms, including akinesia, nighttime pain and spasms, nycturia, dystonia upon awakening, and undesirable psychotic-like effects such as hallucinations [10]. On the other hand, increased daytime sleepiness has been associated to antiparkinsonian drug burden [11, 12], although this relationship remains controversial. Appropriate assessment of sleep problems in PD could contribute to better patient management. The Parkinsons disease sleep scale (PDSS), a visual analogue scale of 15 items, has been developed as a specic clinical tool for assessment of sleep disorders in PD [13]. This scale has been recently recommended for evaluating overall sleep impairment as a screening tool and as a measure of severity by the Sleep Scale Task Force of the Movement Disorder Society [14]. The Task Force recognized that this scale has not been designed for, and is not sufcient to screen for specic sleep disorders in PD such as RLS and RSBD [14]. This study was intended to evaluate prevalence and severity of nighttime sleep disturbances in Italian PD patients, and to validate the Italian version of the PDSS.

Patients and methods This was a multi-center, observational, cross-sectional study with retest. Patients affected by PD and healthy controls were enrolled in seven Italian centres over 16 months. Translation of the original PDSS to Italian language was carried out by two independent professional translators; the translation was examined at a consensus meeting, back-translated and approved at a second consensus meeting. Italian version of the PDSS may be found in Supplementary material. Inclusion criteria for patients and controls were as follows: age ranging between 40 and 80 years, and MiniMental State Examination (MMSE) [15] score C24. Patients had to have a diagnosis of idiopathic PD according to the United Kingdom PD Society Brain Bank Criteria [16] and disease stage 14 on Hoehn & Yahr Modied Scale [17]. Exclusion criteria were as follows: presence of dementia, treatment with sedative or hypnotic medications, severe systemic diseases that might impede adequate assessment of PD and any other kind of inability to understand and complete self-assessment questionnaires. The study was approved by the Ethics Committees of participating centres. Prior to assessments, all subjects signed an informed consent. In order to evaluate the relationship between sleep disorder and dopaminergic treatment, the daily levodopa equivalent dose was calculated for each patient [18].

On the rst visit each subject was asked for the presence of sleep disturbance and then evaluated for cognitive state, depressive symptoms, daytime sleepiness and nighttime sleep quality by means of MMSE [15], Hamilton Depression Rating Scale (HDRS) [19], ESS [20], and PDSS [13]. PD patients were also evaluated by means of Unied PD Rating Scale (UPDRS). Moreover, caregivers were asked for the presence of sudden, jerky and repetitive leg movements and dream-enacting behaviors including talking, punching, kicking, yelling experienced by the patient while asleep, that could resemble PLMS and RSBD, respectively. To evaluate testretest reliability, all patients and controls completed PDSS one week after the rst evaluation, under standardised conditions with the same neurologist administering the scale on each occasion. All the collected data were analysed by means of descriptive statistics. The same descriptive statistics were also calculated in the group of patients split in two classes according to a cut-off value for HDRS (HDRS \17 and HDRS C17) and ESS scales (ESS \12 and ESS C12). Internal consistency of the PDSS scale was evaluated using Cronbachs a coefcients (criterion value C0.70) and item-total corrected correlations (criterion value C0.30). Acceptability was explored by closeness of means to medians (arbitrary limit 10% of the maximum possible score), the ranges of scores, the skewness (limits between -1 and ?1), and the oor and ceiling effect (maximum acceptable for both, 15%). Testretest reliability was assessed using the intraclass correlation coefcient (ICC). ICC values C0.70 were considered satisfactory. Precision was determined by calculating standard error of the measurement (SEM). To assess the sensitivity of the scale in distinguishing between patients and healthy controls, the total and single item scores of the PDSS were compared by using unpaired t test. The concurrent validity of the scale was evaluated analyzing the relation of PDSS with ESS and UPDRS. Correlations between ESS and PDSS scores and age, disease duration, Hoehn & Yahr staging, and type of treatment were examined. Correlation between PDSS total score or single PDSS items scores and levodopa equivalent dose was assessed by means of Spearman coefcients. A stepwise regression model was applied to evaluate the effect of all examined variables on the PDSS and ESS total scores in PD patients. In order to identify general characteristics of sleep disorders pointed out by the PDSS scale (construct validity), a factor analysis model and a cluster analysis model were applied to each item. The opportunity to consider the two questions for the caregiver as additional items of PDSS scale was evaluated. PDSS, ESS, HDRS, and UPDRS total scores were analysed, according to the presence/absence of possible PLMS and RSBD as reported by the caregivers at baseline. To validate the two questions for the caregiver, scores of PDSS items evaluating nocturnal restlessness (items 4 and

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5) and nocturnal psychosis (items 6 and 7) were compared between patients with possible PLMS and RSBD and the remaining patients.

Results We enrolled 221 PD patients (132 M, 89 F; age 66.3 8.9 years) and 57 healthy controls (31 M, 26 F; age 64.5 9.5 years). Sleep disorders were reported by 48% of patients and 19% of controls. PD mean duration was 6.5 4.8 years (range 1 month32 years), and modied H&Y mean stage was 2.3 0.8. Thirty-two percent of the patients were in the initial phase, 39% of patients were in the stable phase and 29% in the complicated phase. Ninety-four percent of patients were treated with antiparkinsonian drugs: 86.8% of them took dopaminergic agonists, 92.7% were on levodopa, 12.2% on amantadine. Mean levodopa equivalent dose was 621 365 mg/day. MMSE scores were similar in PD patients (28.7 2.9) and healthy controls (29.5 1.9). According to HDRS, patients mood was signicantly worse than healthy subjects (mean score 9.6 5.6 vs. 3 3.7; p \ 0.002). Ten percent of PD patients suffered from severe depression (HDRS total score C17). Figure 1 shows proles of mean PDSS scores per item in PD patients and healthy controls at baseline. Table in Supplementary material section shows the differences in total and individual scores of PDSS between PD patients and healthy controls at baseline. Sleep quality was worse in
Table 1 Validation-related statistics in PD patients Cronbachs a

Fig. 1 PDSS proles of mean scores per item in PD patients and healthy controls

patients than in healthy controls: mean total score was 98.3 27.1 in PD patients and 127.9 16.3 in controls (p \ 0.0001). The patients scored about 2 points lower than healthy controls in individual items, and total score difference amounted to approximately 30 points at both visits. PD patients had signicantly lower scores than controls in all items of the PDSS. At the second assessment we observed similar signicant differences between PD patients and controls in total and individual item scores (data not shown). PDSS total score was signicantly lower in PD patients reporting sleep disorders (89.2 28.4) as compared to other PD patients (113.7 22.5; p \ 0.0001). Item proles were similar between the two groups, with item 8 (getting up at night to pass urine) scores being the lowest in each group (Fig. 1). Validation-related statistics are shown in Table 1. Internal consistency of PDSS scale was veried.
Item-total correlation ICC SEM Skewness Floor effect (%) 0 0 0.9 0.45 0.45 0.9 0 0 0.9 0 0 0 0.45 0.45 0 0.45 Ceiling effect (%) 0 0 2.3 0.2 7.2 5.4 6.3 9 2.3 9.9 8.6 8.1 7.7 5.9 1.8 7.7

PDSS total score Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9 Item 10 Item 11 Item 12 Item 13 Item 14 Item 15

0.86 0.85 0.86 0.86 0.85 0.85 0.85 0.86 0.87 0.86 0.85 0.85 0.86 0.86 0.85 0.86 0.65 0.41 0.53 0.57 0.64 0.55 0.46 0.22 0.34 0.65 0.58 0.51 0.39 0.64 0.55

0.96 0.93 0.94 0.88 0.92 0.86 0.88 0.74 0.87 0.82 0.89 0.91 0.82 0.95 0.88 0.91

1.8 0.18 0.22 0.22 0.21 0.23 0.18 0.13 0.22 0.16 0.2 0.21 0.21 0.23 0.22 0.19

-0.44 -0.18 -0.64 0.14 -0.85 -0.38 -0.98 -2.4 0.5 -2.18 -0.86 -0.52 -1.09 -0.66 -0.56 -0.88

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Cronbachs a coefcient value (0.86) indicated highly positive correlations between the items. Item-total corrected correlation showed signicant coefcients for all items. The less correlated item was the eighth (getting up at night to pass urine, r = 0.22). Regarding testretest reliability, the ICC was 0.96 for the total score, which is satisfactory. The ICC for single items ranged from 0.74 (item 7) to 0.95 (item 13) (Table 2). SEM ranged from 0.13 (item 7) to 0.23 (item 5 and 13) and was 1.8 for PDSS total score at both rst and second assessment. Acceptability was good according to all considered criteria. The total PDSS score was free of oor or ceiling effect and the skewness value was -0.44. Negative correlation was found between total PDSS and ESS scores, for both patient and healthy subject groups, at baseline (Table 2) and after one week (data not shown). PDSS scores were approximately 26% lower in patients with relevant daytime sleepiness (ESS C12) than in other PD patients. All items of the PDSS showed a signicant negative correlation with ESS score in PD patients, with the exception of items 2 (falling asleep), 11 (painful cramps) and 13 (tremor on waking) (Table 2). Item 15 of the PDSS showed the greatest correlation coefcient with the total ESS score (r = -0.61, p \ 0.0001). PDSS total score was correlated to PD severity measures: signicant inverse correlation was found between PDSS total score and UPDRS-II and III scores (r = -0.37, p \ 0.0001 and r = -0.26 p = 0.0001). PDSS total score
Table 2 Correlations between PDSS total and individual items scores and ESS total score in PD patients and healthy controls at baseline PDSS Patients R Total score Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9 Item 10 Item 11 Item 12 Item 13 Item 14 Item 15 * p \ 0.05 -0.34 -0.18 -0.03 -0.26 -0.15 -0.16 -0.20 -0.20 -0.30 -0.15 -0.19 -0.11 -0.16 -0.08 -0.25 -0.61 p value \0.0001* 0.0055* 0.5984 \0.0001* 0.0194* 0.0138* 0.0019* 0.0027* \0.0001* 0.0213* 0.0037* 0.0785 0.0146* 0.211 0.0002* \0.0001* Healthy controls r -0.29 -0.26 -0.03 -0.09 -0.11 -0.16 -0.25 -0.02 -0.41 -0.04 -0.14 -0.18 -0.21 -0.08 -0.18 -0.15 p value 0.0455* 0.0749 0.8236 0.5088 0.4356 0.2536 0.0844 0.8549 0.004* 0.7613 0.325 0.2038 0.1476 0.5774 0.2097 0.3106

was inversely related to UPDRS-IV score (r = -0.39; p \ 0.0001). PDSS total score was related to H&Y score (r = -0.27; p \ 0.0001). PDSS total score was found to be signicantly correlated to depression in both groups (r = -0.57, p \ 0.01 for patients and r = -0.53, p \ 0.01 for healthy subjects). PDSS total score was signicantly lower (67 25.1) in patients with HDRS C17 (n = 21) than in patients with HDRS \ 17 (n = 200; 101.5 25.2; p \ 0.001). No correlation was found between levodopa equivalent dose and PDSS total and single item scores in PD patients. Possible PLMS were reported by the caregivers in 36% of PD patients versus 12% of healthy controls (p \ 0.001) while possible RSBD was reported by the caregivers in 27% of PD patients versus 1.7% of healthy controls (p \ 0.001). Patients with possible PLMS as reported by the caregiver scored about 24 points less than other PD patients on PDSS (83.7 25.4 vs. 107.4 23.1; p \ 0.0001). As regards UPDRS-II, mean score was 13.6 7.5 in PD patients with possible PLMS as compared to 10.8 6.4 in patients without (p = 0.005). The presence of possible PLMS was not related to UPDRS-III, MMSE and HDRS scores. Patients with possible PLMS as reported by the caregiver presented signicantly lower scores than PD patients without possible PLMS at item 4 (5.4 3.3 vs. 7.4 3; p = 0.0018) and item 5 (4.2 3.1 vs. 6.7 3.2; p \ 0.001) of the PDSS. PD patients with possible RSBD as reported by the caregiver (27% of PD patients) scored about 16 points less than patients without RSBD on PDSS (86.8 26.2 vs. 102.9 25.5; p \ 0.0001). As regards UPDRS-II, mean score moved from 14.5 8.9 in patients with possible RSBD to 10.8 5.7 in patients without (p \ 0.0001), while UPDRS-III score moved from 27.5 13.1 to 23.5 10.8 (p = 0.026). PD patients with possible RSBD as reported by the caregiver presented signicantly lower scores than PD patients without possible RSBD at item 6 (6 3.1 vs. 8 2.2; p \ 0.0001) and item 7 (7.9 2.3 vs. 8.9 1.5; p \ 0.001) of the PDSS. By regression analysis, we found that presence of motor complications (p = 0.005) and caregivers report of PLMS (p \ 0.0001) were signicant predictors of PDSS, with R2 of 0.22, while female sex (p = 0.0008) and afternoon naps (p = 0.04) were signicant predictors of ESS, with R2 of 0.12. Factor and cluster analysis showed the multidimensional structure of the scale (construct validity). In factor analysis for the patient group, 5 factors were identied, explaining 67% of variance. Factor 1 was related to overall quality of night sleep, including item 1, item 2, item 3, and item 5. Factor 2 was related to nocturnal motor symptoms, including item 4, item 10, item 11, item 12 and item 14. Factor 3 was related in part to nocturnal psychosis,

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including items 6 and 7, and in part to nycturia (item 9) and daytime dozing (item 15). Factor 4 and factor 5 included only one item each one, related to tremor on waking (item 13) and urine incontinence (item 8). In cluster analysis for the patient group, the same conclusions could be drawn, with the difference that the ve clusters explained 63% of total variance. Each cluster was related to the same characteristics of sleep disorders as previous factors with few differences (item 4 in this analysis was included in cluster 2 related to nocturnal motor symptoms).

Discussion Our study showed that the Italian version of the PDSS can be used in routine clinical practice and research. PDSS was able to distinguish between PD patients and controls. Individual items showed good discriminatory power between PD patients and healthy controls. PD patients showed more severe sleep disorders than healthy controls. PDSS was proven time stable and internally consistent in both patient and control groups. Similarly, its internal consistency and testretest reliability were highly satisfactory. The SEM of PDSS was 1.8 for both the crossover and longitudinal assessments, indicating that the Italian version of PDSS is very precise for both crossover and longitudinal studies. Factor analysis showed the multidimensional structure of the scale, with ve factors explaining 67% of variance. Finally, PDSS was able to discriminate between patients with and without reported sleep disturbances. The overall prole of the 15 items was similar to previous reports from England, Spain and Japan [13, 2123]. The mean total PDSS score found in our large sample of PD patients was similar to that reported by Chaudhuri et al. (101.1) [13], Martinez-Martin et al. (96.9) [21], and Abe et al. (99) [22], and lower than those found by Suzuki et al. (112.8) [23], and Wang et al. (118.4) [24]. This discrepancy may reect different composition of the samples among these studies or inter-country differences in sleep disturbances among PD patients. PDSS score was found negatively correlated to ESS score, indicating a relationship between falling asleep during the day and bad quality of night sleep. As found in previous studies [13, 24], poor scores on item 15 (related to daytime naps) of the PDSS were strongly related with excessive daytime sleepiness measured with the ESS, thus supporting criterion validity of the Italian version of PDSS. PDSS scores were negatively correlated to UPDRS section II, III and IV scores, indicating that bad quality of night sleep was related to daily living activities, poor motor function, and the presence of uctuations and dyskinesia. Regression analysis showed that the presence of PLMS as

reported by caregiver and motor complications were signicant, although weak, regressors. Motor complications have been reported to be signicant determinants of sleep disorders also in Japanese and Spanish PD patients [2123], suggesting that nocturnal motor symptoms are relevant in determining bad sleep quality in PD patients. The original version of PDSS does not directly address RSBD and PLMS, which occur frequently in PD. We tried to add two questions for the caregivers that possibly allow for identication of RSBD and PLMS. The report of possible RSBD and PLMS had good discriminatory power between PD patients and healthy controls and was associated with worse sleep quality as indicated by PDSS total scores. Moreover patients with possible PLMS had signicantly worse scores on PDSS items evaluating nocturnal restlessness (items 4 and 5) and patients with possible RSBD had signicantly worse scores on PDSS item evaluating nocturnal psychosis (items 6 and 7), suggesting that these questions could be considered as additional items of the PDSS. A PDSS worse performance was signicantly related also to a worse HDRS score. A correlation between total PDSS scores and measures of anxiety and depression was reported in previous studies [21, 24], and PDSS score has been recently identied as signicant determinant of depression in PD patients [25]. We found no correlation between PDSS score and levodopa equivalent dose. Only one of the previous studies assessing levodopa equivalent dose found a signicant negative correlation with PDSS total score [24], while the majority of previous studies are concordant with our ndings [21, 23, 26]. Limitations of the study are related to characteristics of the samples, particularly regarding the small number of healthy controls and the exclusion of individuals on sedatives or sleeping medication that might have inuenced our results. While our data were in course of analysis, a revised version of the PDSS (PDSS-2) has been proposed and validated in a sample of 113 PD patients from Germany, Austria and England [27]. If the validity and clinical usefulness of this new scale will be conrmed by other studies, it would be worthwhile to validate it in the Italian population.

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